Skip to main content

Advertisement

Log in

Bite Force in Four Pinniped Species from the West Coast of Baja California, Mexico, in Relation to Diet, Feeding Strategy, and Niche Differentiation

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

Behavioral foraging differences are known to aid in food resource partitioning in pinniped communities, but it is not known whether skull biomechanical efficiency also contributes to dietary niche partitioning. We tested this hypothesis in a community of four sympatric species of pinnipeds that co-occur along the coast of Baja California: California sea lion (Zalophus californianus), northern elephant seal (Mirounga angustirostris), harbor seal (Phoca vitulina), and Guadalupe fur seal (Arctocephalus townsendi). We tested whether their preferred prey items differed in resistivity to puncture and whether those differences were linked to the mass of the muscles of mastication and the biomechanical efficiency with which they can puncture prey items. For each prey species, we measure resistivity to puncture using texture profile analysis. We found that M. angustirostris consumes the most resistant prey and that A. townsendi consumes the least resistant. We estimated physiological cross-sectional area of the muscles of mastication for each pinniped and found that the same pair of species respectively has the largest and smallest theoretical value of muscular force. Finally, we estimated the bite force that each pinniped species requires to puncture its prey by solving Euler-Lagrange equations based on biomechanical lever model parameters measured from 3D digital models of the skulls. We also found differences in efficiency between the species. These data allowed us to classify the three ecomorphological types. Type 1 features a hydrodynamic skull with relatively low mandibular forces, characteristic of pelagic carnivore feeders such as A. townsendi. Type 2, represented by Z. californianus and M. angustirostris (both opportunistic feeders), is characterized by broad insertion areas for the mandibular muscles and strong teeth, permitting these predators to vary the prey target species as a function of prey availability. Type 3 features a less robust skull and a lower muscle efficiency, characteristic of benthic feeders such as P. vitulina. This evidence indicates that biomechanical differences between the species contribute to dietary niche construction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adam PJ, Berta A (2001) Evolution of prey capture strategies and diet in the Pinnipedimorpha (Mammalia, Carnivora). Oryctos 4:83–107.

    Google Scholar 

  • Aguirre LF, Herrel A, van Damme R, Matthysen E (2002) Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proc R Soc Lond Ser B 269:1271–1278

    Google Scholar 

  • Anderson PSL, Rayfield EJ (2012) Virtual experiments, physical validation: dental morphology at the intersection of experiment and theory. J R Soc Interface 9:1846–1855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Attard MRG, Parr WCH, Wilson LAB, Archer M, Hand SJ, Rogers TL, Wroe S (2014) Virtual reconstruction and prey size preference in the Mid Cenozoic thylacinid, Nimbacinus dicksoni (Thylacinidae, Marsupialia). PLoS ONE 9(4):e93088

  • Aurioles-Gamboa D, Camacho-Ríos FJ (2007) Diet and feeding overlap of two otariids, Zalophus californianus and Arctocephalus townsendi: implications to survive environmental uncertainty. Aquat Mammal 33(3):317–326

  • Campbell KM, Santana SE (2017) Do differences in skull morphology and bite performance explain dietary specialization in sea otters? J Mammal 98(5):1408–1416

  • Christiansen P (2007) Evolutionary implications of bite mechanics and feeding ecology in bears. J Zool 272: 423–443

    Google Scholar 

  • Christiansen P, Adolfssen JS (2005) Bite forces, canine strengths and skull allometry in extant carnivores (Mammalia, Carnivora). J Zool Lond 266:1–19

    Google Scholar 

  • Christiansen P, Wroe S (2007) Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology 88:347–358

    PubMed  Google Scholar 

  • Condit R, Le Boeuf BJ (1984) Feeding habits and feeding grounds of the northern elephant seal. J Mammal 65:281–290

    Google Scholar 

  • Conlan C (2017) The Blender Phyton API: Precision 3D Modeling and Add-on Development. Apress, New York

    Google Scholar 

  • Damasceno EM, Hingst-Zaher E, Astúa D (2013) Bite force and encephalization in the Canidae (Mammalia: Carnivora). J Zool 290:246–254

    Google Scholar 

  • Dassault Systèmes (2012) CATIA V6 (computer-aided three dimensional interactive application). Dassault Systèmes SolidWorks Corporation, Vélizy-Villacoublay Cedex, France

    Google Scholar 

  • Davis JL, Santana SE, Dumont ER, Grosse IR (2010) Predicting bite force in mammals: two-dimensional versus three-dimensional lever models. J Exp Biol 213:1844–1851

  • Drago M (2010) Dieta y dinámica poblacional del león marino del sur (Otaria flavescens) en Patagonia. PhD Dissertation, Universitat de Barcelona, Spain

  • Druzinsky RE, Doherty AH, De Vree FL (2011) Mammalian masticatory muscles: homology, nomenclature, and diversification. Integr Comp Biol 51(2):224–234

    PubMed  Google Scholar 

  • Dumont ER (1999) The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study. J Zool 248:219–29

    Google Scholar 

  • Dumont ER, Herrel A (2003) The effects of gape angle and bite point on bite force in bats. J Exp Biol 206:2117–2123

    PubMed  Google Scholar 

  • Dumont ER, Herrel A, Medellin RA, Vargas J, Santana SE (2009) Built to bite: cranial design and function in the wrikle faced bat (Centurio senex). J Zool 279:329–337

  • Dunajski E (1980) Texture of fish muscle. J Texture Stud 10(4):301–318

    CAS  Google Scholar 

  • Emmons LH (1987) Comparative feeding ecology of felids in a Neotropical rainforest. Behav Ecol Sociobiol 20:271–283

    Google Scholar 

  • Eng CM, Ward SR, Vinyard CJ, Taylor AB (2009) The morphology of the masticatory apparatus facilitates muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus). J Exp Biol 212:4040–4055

  • Errickson D, Grueso I, Griffith SJ, Setchell JM, Thompson TJU, Thompson CEL, Gowland RL (2017) Towards a best practice for the use of active non-contact surface scanning to record human skeletal remains from archaeological contexts. Int J Osteoarchaeol 27(4):650–661

    Google Scholar 

  • Erickson GM, Lappin AK, Vliet KA (2003) The ontogeny of bite-force performance in American alligator (Alligator mississippiensis). J Zool Lond 260:317–327

  • Errickson D, Thompson TJU, Rankin BWJ (2015) An optimum guide for the reduction of noise using a surface scanner for digitising human osteological remains. http://guides.archaeologydataservice.ac.uk/g2gp/CS_StructuredLight

  • Espinosa de los Reyes MG (2007) Variabilidad espacial de la dieta del lobo marino de California (Zalophus californianus californianus, Lesson 1828). MSc thesis, Centro de Investigación Científica y de Educación Superior de Ensenada. Ensenada, Baja California, México

  • Fernández-Díaz MD, Montero P, Gómez-Guillén MC (2003) Effect of freezing fish skins on molecular and rheological properties of extracted gelatin. Food Hydrocoll 17:281–286

    Google Scholar 

  • Gallo-Reynoso JP, Figueroa-Carranza AL (1992) A cookiecutter shark wound on a Guadalupe fur seal male. Mar Mammal Sci 8(4):828–830

    Google Scholar 

  • García-Rodríguez FJ, Aurioles-Gamboa D (2004) Spatial and temporal variation in the diet of the California sea lion (Zalophus californianus) in the Gulf of California, Mexico. Fish Bull 102: 47–62

  • Germain LR, McCarthy MD, Koch PL, Harvey JT (2011) Stable carbon and nitrogen isotopes in multiple tissues of wild and captive harbor seals (Phoca vitulina) off the California coast. Mar Mammal Sci 28(3):542–560

  • Ghazali M, Dzeverin I (2013) Correlations between hardness of food and craniodental traits in nine Myotis species (Chiroptera, Vespertilionidae). Vestn Zool 47(1):73–82

  • González-Suárez M, Cassini MH (2013) Variance in male reproductive success and sexual size dimorphism in pinnipeds: testing an assumption of sexual selection theory. Mammal Rev 44(2):88–93

    Google Scholar 

  • Grünheid T, Langenbach GEJ, Korfage JAM, Zentner A, van Eijden TMGJ (2009) The adaptive response of jaw muscles to varying functional demands. Eur J Orthod 31(6):596–612

    PubMed  Google Scholar 

  • Gulka J, Ronconi RA, Davoren GK (2019) Spatial segregation contrasting dietary overlap: niche partitioning of two sympatric alcids during shifting resource availability. Mar Biol 166:115

    Google Scholar 

  • Herrel A, De Smet A, Aguirre LF, Aerts P (2008a) Morphological and mechanical determinants of bite force in bats: do muscle matter? J Exp Biol 211:86–91

    PubMed  Google Scholar 

  • Herrel A, Holanova V (2008) Cranial morphology and bite force in Chamaeleolis lizards – Adaptations to molluscivory? Zoology 111:467–475

    PubMed  Google Scholar 

  • Herrel A, De Smet A, Aguirre LF, Aerts P (2008b) Morphological and mechanical determinants of bite force in bats: do muscle matter? J Exp Biol 211:86–91

  • Hocking DP, Evans AR, Fitzgerald EMG (2013) Leopard seals (Hydrurga leptonyx) use suction and filter feeding when hunting small prey underwater. Polar Biol 36(2):211–222

  • Hocking DP, Salverson M, Fitzgerald EMG, Evans AR (2014) Australian fur seals (Arctocephalus pusillus doriferus) use raptorial biting and suction feeding when targeting prey in different foraging scenarios. PLoS ONE 9(11):e112521

  • Hylander WL, Johnson KR, Crompton AW (1992) Muscle force recruitment and biomechanical modeling: an analysis of masseter muscle function during mastication in Macaca fascicularis. Am J Phys Anthropol 88(3):365–387

  • Jones KE, Goswami A (2010) Quantitative analysis of the influences of phylogeny and ecology on phocid and otariid pinniped (Mammalia; Carnivora) cranial morphology. J Zool 280:297–308

    Google Scholar 

  • Jones KE, Ruff CB, Goswami A (2013) Morphology and biomechanics of the pinniped jaw: mandibular evolution without mastication. Anat Record 296:1049–1063

    Google Scholar 

  • Jones M (2003) Convergence in ecomorphology and guild structure among marsupial and placental carnivores. In: Jones M, Dickman C, Archer M (eds) Predators with Pouches: the Biology of Carnivorous Marsupials. CSIRO Publishing, Collingwood, pp 285–296

    Google Scholar 

  • Kemp TS (2005) The Origin and Evolution of Mammals. Oxford University Press, Oxford

    Google Scholar 

  • Kienle SS, Berta A (2016) The better to eat you with: the comparative feeding morphology of phocid seals (Pinnipedia, Phocidae). J Anat 228(3):396–413

  • Kiltie RA (1988) Interspecific size regularities in tropical felid assemblages. Oecologia 76(1):97–105

    CAS  PubMed  Google Scholar 

  • Kleinteich T, Haas A, Summers AP (2008) Caecilian jaw-closing mechanics: integrating two muscle systems. J R Soc Interface 5:1491–1504

    PubMed  PubMed Central  Google Scholar 

  • Law CJ, Mehta RS (2019) Dry versus wet and gross: comparisons between the dry skull method and gross dissection in estimations of jaw muscle cross-sectional area and bite forces in sea otters. J Morphol 280:1706–1713

    PubMed  Google Scholar 

  • Ledogar JA, Winchester JM, St Clair EM, Boyer DM (2013) Diet and dental topography in pitheciine seed predators. Am J Phys Anthropol 150:107–121

    PubMed  Google Scholar 

  • Leonard KC, Boettcher ML, Dickisnson E, Malhotra N, Aujard F, Herrer A, Harstone-Rose A (2019) The ontogeny of masticatory muscle architecture in Microcebus murinus. Anat Rec 24259

  • Maie T, Schoenfuss HL, Blob RW (2009) Jaw lever analysis of Hawaiian gobioid stream fishes: a simulation study of morphological diversity and functional performance. J Morphol 270:976–983

    PubMed  Google Scholar 

  • Marshall CD Goldbogen JA (2015) Feeding mechanisms. In: Castellini M, Mellish J (eds) Marine mammal physiology: requisites for ocean living. CRC Press, Boca Raton, pp 95–118

    Google Scholar 

  • Marshall CD, Pyenson ND (2019) Feeding in aquatic mammals: an evolutionary and functional approach. In: Bels V, Whishaw IQ (eds) Feeding in vertebrates: anatomy, biomechanics, evolution. Springer International Publishing, pp 743–785

  • Marshall CD, Wieskotten S, Hanke W, Hanke FD, Marsh A, Kot B, Dehnhardt G (2014) Feeding kinematics, suction, and hydraulic jetting performance of harbor seals (Phoca vitulina). PLoS ONE 9(1):e86710

  • McMahon TA (1984) Muscles, reflexes, and locomotion. Princeton University Press, Princeton

    Google Scholar 

  • Meriam JL, Kraige LG, Palm WJ (2002) Engineering Mechanics: Dynamics. John Willey and Sons, New York

    Google Scholar 

  • Metzger KA (2009) Quantitative analysis of the effect of prey properties on feeding kinematics in two species of lizards. J Exp Biol 212:3751–3761

    PubMed  Google Scholar 

  • Mischa K (2020) Euler-Lagrange tool package. (https://www.mathworks.com/matlabcentral/fileexchange/49796-euler-lagrange-tool-package), MATLAB Central File Exchange. Retrieved February, 2018

  • Nogueira MR, Peracchi AL, Monteiro LR (2009) Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Funct Ecol 23:715–723

    Google Scholar 

  • Orr AJ, VanBlaricom GR, DeLong RL, Cruz-Escalona VH, Newsome SD (2011) Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses. Can J Zool 89:109–122

    CAS  Google Scholar 

  • Pablo-Rodríguez N (2009) Amplitud, nivel y superposición trófica de los pinnípedos de Islas San Benito B.C. México. MSc Thesis. Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marina. La Paz, Baja California Sur, México

  • Porras-Peters H, Aurioles-Gamboa D, Cruz-Escalona VH, Koch PL (2008) Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico. Mar Mammal Sci 24(3):554–576

    Google Scholar 

  • Radinsky LB (1981) Evolution of skull shape in carnivores. Biol J Linnean Soc 15:369–388

    Google Scholar 

  • Rahmat SJ, Koretsky IA (2015) Diversity of mandibular morphology in some carnivorans. Vestn Zool 49(3):267–284

    Google Scholar 

  • Riedman M (1990) The Pinnipeds: Seals, Sea Lions and Walruses. University of California Press, Berkeley

    Google Scholar 

  • Sakamoto M, Lloyd GT, Benton MJ (2010) Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance. J Evol Biol 23:463–478

    CAS  PubMed  Google Scholar 

  • Santana SE, Dumont ER (2009) Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats. J Evol Biol 22:2131–2145

    CAS  PubMed  Google Scholar 

  • Santana SE, Dumont ER, Davis JL (2010). Mechanics of bite force production and its relationship to diet in bats. Func Ecol 24:776–784

    Google Scholar 

  • Taylor AB, Vogel ER, Dominy NJ (2008) Food material properties and mandibular load resistance abilities in large-bodied hominoids. J Hum Evol 55:604–616

    PubMed  Google Scholar 

  • Thomason JJ (1991) Cranial strength in connection with estimated biting forces in some mammals. Can J Zool 69:2326–2333

    Google Scholar 

  • Thompson U, Norris P (2018) A new method for the recovery and evidential comparison of footwear impressions using 3D structured light scanning. Sci Justice 58:237–243

    CAS  PubMed  Google Scholar 

  • Tipler PA, Mosca G (2004) Physics for Scientists and Engineers. Vol. 1 Mechanics, Oscillations and Waves, Thermodynamics. W. H. Freeman and Company, New York

  • Turnbull WB (1970) Mammalian masticatory apparatus. Fieldiana Geol 18(2):149–356

    Google Scholar 

  • Van Soest PJ (1996) Allometry and ecology of feeding behavior and digestive capacity in herbivores: a review. Zoo Biol 15(5):455–479

    Google Scholar 

  • Vanhooydonck B, Herrel A, Van Damme R (2007) Interactions between habitat use, behavior, and the trophic niche of lacertid lizards. In: Reilly SM, McBrayer LD, Miles DB (eds) Lizard ecology: the evolutionary consequences of foraging mode. Cambridge University Press, Cambridge, pp 427–449

    Google Scholar 

  • Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 42–59

    Google Scholar 

  • Weijs WA (1980) Biomechanical models and the analysis of form: a study of the mammalian masticatory apparatus. Am Zool 20:707–719

  • Weijs WA, Hillen B (1985) Physiological cross-section of the human jaw muscles. Acta anat 121:31–35

  • Westneat MW (2006) Mandibular lever mechanics. MandibLever 3.2. Department of Zoology. Chicago: Field Museum of Natural History

  • Westneat MW (2010) MandibLever 3.3. Department of Zoology. Field Museum of Natural History, Chicago

  • Williams SH, Peiffer E, Ford S (2009) Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: does jaw-muscle anatomy predict performance? J Morphol 270: 1338–1347

    PubMed  Google Scholar 

Download references

Acknowledgments

Research funded by a grant of the Consejo Nacional de Ciencia y Tecnología to RAFM (CONACyT fellowship: 298549). Thanks to Mark S. Peterson, Stephan Lautenschlager, Jorge A. del Ángel-Rodríguez, John Wible, and three anonymous reviewers for critical review of the manuscript. RAM is a fellow recipient of the Consejo Nacional de Ciencia y Tecnología (CONACYT)-Secretaría de Energía (SENER)-Hidrocarburos (Project 201441). RAM, EMM, GHC, and VHCE are fellowships recipients of the Sistema Nacional de Investigadores (CONACyT-SNI). GHC and VHCE are grateful for the support from EDI and COFAA IPN Programs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Víctor Hugo Cruz-Escalona.

Electronic supplementary material

ESM 1

(XLSX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franco-Moreno, R.A., Polly, P.D., Toro-Ibacache, V. et al. Bite Force in Four Pinniped Species from the West Coast of Baja California, Mexico, in Relation to Diet, Feeding Strategy, and Niche Differentiation. J Mammal Evol 28, 307–321 (2021). https://doi.org/10.1007/s10914-020-09524-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-020-09524-7

Keywords

Navigation